RESEARCH ARTICLE Living with relatives offsets the harm caused by pathogens in natural populations Hanna M Bensch, Emily A O’Connor, Charlie Kinahan Cornwallis* Department of Biology, Lund University, Lund, Sweden Abstract Living with relatives can be highly beneficial, enhancing reproduction and survival. High relatedness can, however, increase susceptibility to pathogens. Here, we examine whether the benefits of living with relatives offset the harm caused by pathogens, and if this depends on whether species typically live with kin. Using comparative meta-analysis of plants, animals, and a n bacterium ( species = 56), we show that high within-group relatedness increases mortality when pathogens are present. In contrast, mortality decreased with relatedness when pathogens were rare, particularly in species that live with kin. Furthermore, across groups variation in mortality was lower when relatedness was high, but abundances of pathogens were more variable. The effects of within-group relatedness were only evident when pathogens were experimentally manipulated, suggesting that the harm caused by pathogens is masked by the benefits of living with relatives in nature. These results highlight the importance of kin selection for understanding disease spread in natural populations. Introduction High relatedness between individuals can favour the evolution of cooperative interactions that increase reproductive success and survival (Hamilton, 1964a; Hamilton, 1964b). For example, it has been repeatedly shown that individuals can pass on their genes indirectly by providing vital resour- *For correspondence: ces to relatives and assisting them with tasks that are difficult to do alone, such as caring for off- [email protected] spring (Alexander, 1974; Rubenstein and Abbot, 2017; West et al., 2007). However, living with relatives can also increase susceptibility to pathogens that spread more easily among genetically Competing interests: The similar individuals, with similar immune defences (Anderson et al., 1986; Baer and Schmid-Hempel, authors declare that no 1999; Hamilton, 1987; Liersch and Schmid-Hempel, 1998; Schmid-Hempel, 1998; Sherman et al., competing interests exist. 1998). This phenomenon has been referred to as the ‘monoculture effect’ (Elton, 1958) in agricul- Funding: See page 15 tural settings after it was observed that clonal crops were highly susceptible to disease outbreaks Received: 18 January 2021 (Garrett and Mundt, 1999; Tooker and Frank, 2012; Wolfe, 1985; Zhu et al., 2000). More Accepted: 19 June 2021 recently it has also been established that such effects occur in natural populations, with higher Published: 26 July 2021 genetic similarity between individuals increasing rates of parasitism (Ekroth et al., 2019). What Reviewing editor: Dieter Ebert, remains unclear is whether this translates into higher rates of mortality, or whether the benefits of liv- University of Basel, Switzerland ing with relatives are large enough to offset the costs of increased disease risk (Hughes et al., 2002). Copyright Bensch et al. This Previous research into the effects of relatedness on disease spread have been conducted on an article is distributed under the expansive range of species including bacteria, plants, and animals. These studies have revealed terms of the Creative Commons Attribution License, which remarkable variation in how changes in relatedness influence parasitism and mortality. For example, permits unrestricted use and in honeybees, Apis melifera, high relatedness among individuals increases the risk of disease and redistribution provided that the colony death (Tarpy et al., 2013), whereas in Pharoah ants, Monomorium pharaonis, high related- original author and source are ness reduces the abundance of pathogens (Schmidt et al., 2011). Such differences between species credited. may in part be due to how data are collected. In some studies, relatedness and pathogens have Bensch et al. eLife 2021;10:e66649. DOI: https://doi.org/10.7554/eLife.66649 1 of 24 Research article Ecology Evolutionary Biology eLife digest Living in a group with relatives has many advantages, such as helping with child rearing and gathering food. This has led many species to evolve a range of group behaviours; for example, in honey bee populations, worker bees sacrifice themselves to save the colony from incoming enemies. But there are also downsides to living with family. For example, bacteria, viruses and other disease-causing pathogens will find it easier to spread between relatives. This is because individuals with the same genes have similar immune defences. So, is it better to live with relatives who can help with life’s struggles or live with unrelated individuals where there is a lower chance of getting sick? To help answer this question, Bensch et al. analysed data from 75 studies which encompassed 56 different species of plants, animals, and one type of bacteria. This showed that creatures living in family groups experienced more disease and had a higher risk of death. However, if groups had a low chance of encountering pathogens, individuals living with relatives were more likely to survive. This cancels out the disadvantages family groups face when pathogens are more common. The analysis by Bensch et al. provides new insights into how pathogens spread in species with different social systems. This information can be used to predict how diseases occur in nature which will benefit ecologists, epidemiologists, and conservation biologists. been experimentally manipulated, whereas in other studies relatedness and the abundances of pathogens are only observed (‘observational studies’). In observational studies, results can be vari- able and difficult to interpret because the causality behind relationships is uncertain (Lively et al., 2014). For instance, a negative relationship between relatedness and the abundance of pathogens can occur either because groups of relatives are less susceptible to pathogens, or because groups of relatives die from pathogens and so are rarely observed (Ben-Ami and Heller, 2005; King et al., 2011; Teacher et al., 2009). Additionally, species may vary in their susceptibility to pathogens because of differences in past selection to control disease spread among individuals (Loehle, 1995; Romano et al., 2020). In spe- cies where relatives frequently interact, selection is predicted to favour the evolution of strategies that mitigate the impacts of pathogens (Loehle, 1995; Romano et al., 2020). Limiting social interac- tion through group-level organisation, such as task partitioning and other mechanisms of the so- called ‘social immunity’, can prevent disease spread among relatives (Camargo et al., 2007; Cremer and Sixt, 2009; Liu et al., 2019; Ugelvig et al., 2010; Waddington and Hughes, 2010). However, whether species that typically live with kin are better able to cope with pathogens when relatives interact, compared to species that live with non-kin, is unclear. The spread of disease through populations also depends on how variable pathogen abundances are across groups. Pathogen abundances are expected to be more variable among groups of rela- tives because they either contain resistant or susceptible genotypes (Boomsma and Ratnieks, 1996; van Baalen and Beekman, 2006). Groups of unrelated individuals, on the other hand, will contain a mix of susceptible and resistant genotypes, leading to more predictable pathogen abundances and rates of mortality across groups. Such differences in variation across groups of related and unrelated individuals are nevertheless predicted to depend on pathogen diversity. When there are many differ- ent pathogens, groups of relatives are more likely to be susceptible to at least one pathogen, which can reduce variation in total pathogen abundance to a level that is similar to groups of unrelated individuals (Ganz and Ebert, 2010; van Baalen and Beekman, 2006). While both increases and decreases in variation in rates of parasitism and mortality have been found in specific study species (Ganz and Ebert, 2010; Johnson et al., 2006; Seeley and Tarpy, 2007; Thonhauser et al., 2016), whether variation among groups of relatives is generally higher across species remains to be tested. Here, we use phylogenetic meta-analysis to first examine whether the benefits of living with rela- tives counteract the costs of increased susceptibility to pathogens. Second, we tested if the ability to detect such effects is dependent upon the experimental manipulation of pathogens and within- group relatedness. Third, we examined if species that typically live with kin have evolved mecha- nisms to reduce pathogen spread among relatives compared to species that typically live with non- Bensch et al. eLife 2021;10:e66649. DOI: https://doi.org/10.7554/eLife.66649 2 of 24 Research article Ecology Evolutionary Biology kin. Finally, we investigated whether variation in the abundance of pathogens and rates of mortality is higher across groups of relatives. The influence of relatedness on mortality and pathogen abun- dances were quantified by extracting effect sizes (Pearson’s correlation coefficients r) from 75 pub- lished studies across 56 species (Supplementary file 1—Tables S1-S3). Variation in pathogen abundances and rates of mortality were measured using a standardised effect size of variance that accounts for differences in means, the coefficient of variation ratio (CVR), which was possible to esti- mate for 25 species (Supplementary file 1—Table S4). Results Relatedness and susceptibility